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Perspectives from Reticulate Evolution Abstract Introduction Preprints (www.preprints.org) | NOT PEER-REVIEWED | Posted: 21 April 2021 Wheat speciation and adaptation: perspectives from reticulate evolution Authors Xuebo Zhao1,2, Xiangdong Fu1,2, Changbin Yin1,*, Fei Lu1,2,3,* Affiliations 1State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing, China. 2University of Chinese Academy of Sciences, Beijing, China. 3CAS-JIC Centre of Excellence for Plant and Microbial Science (CEPAMS), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China. Correspondence [email protected] (F.L.); [email protected] (C.Y.) Abstract Reticulate evolution through the interchanging of genetic components across organisms can impact significantly on the fitness and adaptation of species. Bread wheat (Triticum aestivum subsp. aestivum) is one of the most important crops in the world. Allopolyploid speciation, frequent hybridization, extensive introgression, and occasional horizontal gene transfer (HGT) have been shaping a typical paradigm of reticulate evolution in bread wheat and its wild relatives, which is likely to have a substantial influence on phenotypic traits and environmental adaptability of bread wheat. In this review, we outlined the evolutionary history of bread wheat and its wild relatives with a highlight on the interspecific hybridization events, demonstrating the reticulate relationship between species/subspecies in the genera Triticum and Aegilops. Furthermore, we discussed the genetic mechanisms and evolutionary significance underlying the introgression of bread wheat and its wild relatives. An in-depth understanding of the evolutionary process of Triticum species should be beneficial to future genetic study and breeding of bread wheat. Keywords: wheat; reticulate evolution; introgression; speciation; hybridization; adaptation; breeding Introduction The ‘tree of life’ is a classic paradigm representing the evolution of life and illustrating the relationship of species1. While being practical and useful, the tree-like model can be incomplete because fusion, transfer, and exchange of DNA between species can form a net-like evolutionary relationship, shaping the paradigm of reticulate evolution2. Recently, a growing body of research shows that reticulate evolution is common in nature – hybridization, gene flow, and polyploidization were identified in multiple species of humans3–6, animals7–15, and plants16–20. The drastic turnover of genetic components brings forth rapid changes of genetic © 2021 by the author(s). Distributed under a Creative Commons CC BY license. Preprints (www.preprints.org) | NOT PEER-REVIEWED | Posted: 21 April 2021 diversity, diversification, and speciation, establishing a new fitness landscape of species7,14. For crops, gene flow through reticulate evolution can be a valuable resource to investigate genetic mechanisms and candidate genes of crops adapting to various environments21. Wheat cultivation began from the Neolithic Age. Over the past few thousand years, wheat was of extreme importance as a staple food that facilitated human civilization development22. In the present-day, wheat has become the second most-produced cereal crop and the most widely grown crop in the world, contributing ~20% of the calories and proteins to the human diet23. However, climate models predict an acceleration of environmental extremes in near future, which are probably the prelude to a subsequent shortage of agricultural supply worldwide24. Moreover, the climate resilience of wheat was found declining in most European countries during the last 10 years, probably due to the reduced diversity in the genetic pool of cultivars25,26. Improving the ability of crops to cope with both biotic and abiotic stresses will likely play an important role in the adaptation of agriculture to climate change in the coming decades27,28. To address the agricultural challenges of this century, there is a pressing demand to understand the adaptive evolution of wheat and its wild relatives, and better utilize the gene pool of wheat. Reticulate evolution of wheats (Triticum species) has long been recognized. The speciation of wheats is a classic example of reticulate evolution through allopolyploidization, shaping tetraploid and hexaploid species in the genus Triticum29–31. Two economically important wheats are bread wheat (Triticum aestivum subsp. aestivum, AABBDD, 2n = 6x = 42) and durum wheat (T. turgidum subsp. durum, AABB, 2n = 4x = 28), comprising 95% and 5% of the global wheat production, respectively32,33. Research of wheat evolution has focused primarily on two successive rounds of polyploidization events of bread wheat34,35. Homoploid hybridization, introgression, and their biological significance received considerably less attention. Recent studies showed that bread wheat received introgression from their wild relatives, facilitating its adaptation to new environments30,31 and resistance to biotic stress36. The benefits of wild species as readily available resources of adaptive alleles are getting recognized37. Here, we review the process of reticulate evolution of Triticum species, then discuss the biological significance of reticulate evolution in bread wheat and its wild relatives, with a highlight on the impact of introgression upon global adaptation of wheat. Phylogenetic tree of Triticum species The Triticum-Aegilops alliance, which contains the direct genetic donors of bread wheat, belongs to the tribe Triticeae. The tribe Triticeae emerging about 25 million years ago (Mya), was split into two subtribes, Hordeineae and Triticineae, about 15 million years ago38,39. Triticineae is an economically important subtribe, giving rise to the domesticated cereals of wheat, rye, and several important forage grass33 (Fig. 1A). Bread wheat and its closely related species (Table 1) include 9 species and 29 subspecies, growing mostly in temperate zones, principally in the northern hemisphere40,41. These subspecies are annuals and have solitary spikelet, with their original habitats in the eastern Mediterranean, and the cradle of agriculture– Fertile Crescent42,43. Preprints (www.preprints.org) | NOT PEER-REVIEWED | Posted: 21 April 2021 Table 1 The nomenclature and main traits of bread wheat and their wild relatives in Triticum and Aegilops Genome Pollination Reference Brittle Free- Names in this review Species Subspecies Breeding state constitution mode* genome rachis threshing (common name) Ae. speltoides Ae. speltoides subsp. speltoides SS C No Wild Yes No Speltoides Tausch Ae. speltoides subsp. ligustica (Savign.) Zhuk. SS C No Wild Yes No Ligustica Ae. tauschii Coss. subsp. strangulata DD S Yes Wild Yes No Strangulata Ae. tauschii Ae. tauschii Coss. subsp. tauschii DD S No Wild Yes No Tauschii T. monococcum L. subsp. aegilopoides (Link) Thell. AA S No Wild Yes No Wild einkorn T. monococcum T. monococcum L. subsp. monococcum AA S No Domesticated No No Domesticated einkorn T. sinskajae T. sinskajae A.Filat. & Kurk. subsp. sinskajae AA S No Domesticated No No Sinskaya T. urartu T. urartu Tumanian ex Gandilyan AA S Yes Wild Yes No Urartu T. turgidum L. subsp. dicoccoides (Korn. ex Asch. & Graebn.) Thell. AABB S Yes Wild No No Wild emmer T. turgidum L. subsp. dicoccon (Schrank) Thell. AABB S No Domesticated No No Domesticated emmer T. karamyschevii NEVSKI var. karamyschevii AABB S No Domesticated No No Georgian wheat T. ispahanicum Heslot AABB S No Domesticated No No Ispahanicum T. turgidum T. turgidum L. subsp. turgidum AABB S No Domesticated No Yes Rivet wheat T. turgidum L. subsp. polonicum (L.) Thell. AABB S No Domesticated No Yes Polish wheat T. turgidum L. subsp. carthlicum (Nevski) A. Love & D. Love AABB S No Domesticated No Yes Persian wheat T. turgidum L. subsp. turanicum (Jakubz.) A. Love & D. Love AABB S No Domesticated No Yes Khorasan wheat T. turgidum L. subsp. durum (Desf.) Husn. AABB S Yes Domesticated No Yes Durum T. timopheevii subsp. armeniacum (Jakubz.) van Slageren AAGG S No Wild Yes No Wild timopheevii T. timopheevii T. timopheevii subsp. timopheevii AAGG S No Domesticated No No Domesticated timopheevii T. aestivum L. subsp. spelta (L.) Thell. AABBDD S Yes Wild/Domesticated No No Spelt T. aestivum L. subsp. macha (Dekapr. & Menabde) Mackey AABBDD S No Wild/Domesticated No No Macha T. aestivum L. subsp. compactum (Host) Mackey AABBDD S No Domesticated No Yes Club wheat T. aestivum L. subsp. sphaerococcum (Percival) MacKey AABBDD S No Domesticated No Yes Indian dwarf wheat T. aestivum T. aestivum subsp. yunanense AABBDD S No Domesticated No No Yunan wheat T. petropavlovskyi Udachin & Migush. AABBDD S No Domesticated No Yes Xinjiang wheat T. aestivum subsp. tibetanum AABBDD S No Wild/Domesticated Yes No Tibetan semi-wild T. vavilovii (Tumanian) Jakubz. var. vavilovii AABBDD S No Wild/Domesticated No Yes Vavilovii T. aestivum L. subsp. aestivum AABBDD S Yes Domesticated No Yes Bread wheat T. zhukovskyi T. zhukovskyi Menabde & Ericz. AAAAGG S No Wild No No Zhukovskyi Source: Wheat Genetics Resource Center (https://www.k-state.edu/wgrc/genetic_resources/triticum_accessions/index.html). * C cross-pollination, S self-pollination During the speciation of bread wheat, the first hybridization occurred ~0.8 Mya between close relatives (BB) of Ae. speltoides and T. urartu (AA), giving rise to the allotetraploid wild emmer wheat (T. turgidum subsp. dicoccoides, AABB) by polyploidization. At the beginning of agriculture in the Fertile
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